Leishmania infantum xenodiagnosis from vertically infected dogs reveals significant skin tropism

Abstract

Background Dogs are the primary reservoir for human visceral leishmaniasis due to Leishmania infantum. Phlebotomine sand flies maintain zoonotic transmission of parasites between dogs and humans. A subset of dogs is infected transplacentally during gestation, but at what stage of the clinical spectrum vertically infected dogs contribute to the infected sand fly pool is unknown. Methodology/Principal findings We examined infectiousness of dogs vertically infected with L. infantum from multiple clinical states to the vector Lutzomyia longipalpis using xenodiagnosis and found that vertically infected dogs were infectious to sand flies at differing rates. Dogs with mild to moderate disease showed significantly higher transmission to the vector than dogs with subclinical or severe disease. We documented a substantial parasite burden in the skin of vertically infected dogs by RT-qPCR, despite these dogs not having received intradermal parasites via sand flies. There was a highly significant correlation between skin parasite burden at the feeding site and sand fly parasite uptake. This suggests dogs with high skin parasite burden contribute the most to the infected sand fly pool. Although skin parasite load and parasitemia correlated with one another, the average parasite number detected in skin was significantly higher compared to blood in matched subjects. Thus, dermal resident parasites were infectious to sand flies from dogs without detectable parasitemia. Conclusions/Significance Together, our data implicate skin parasite burden and earlier clinical status as stronger indicators of outward transmission potential than blood parasite burden. Our studies of a population of dogs without vector transmission highlights the need to consider canine vertical transmission in surveillance and prevention strategies.

Clinical and parasitological impact of short-term treatment using miltefosine and allopurinol monotherapy or combination therapy in canine visceral leishmaniasis

“…The skin is the site of the first interaction between Leishmania and the host's immune system, and parasite detection in the skin samples is possible even in clinically healthy patients (Ciaramella et al, 1997). According to Scorza et al (2021), the amount of parasite DNA in the skin is more relevant than the dog's clinical status.…”

“…However, the disease has adapted to the urban environment due to environmental changes, such as deforestation and urbanization (Santos et al, 2021). Due to the adaptation of the sand fly to the domestic environment, dogs have become the main source of infection for humans in urban areas (Marcondes & Day, 2019;Scorza et al, 2021).…”

“…The most common clinical signs include skin lesions such as ulcers, alopecia, and scaling, lymphadenomegaly, anorexia, muscle atrophy, lethargy, splenomegaly, eye lesions, onychogryphosis, lameness, vomiting, and diarrhea (Ciaramella et al, 1997;Solano-Gallego et al, 2009). Even when clinical signs are absent, infected dogs can exhibit severe cutaneous parasitism with infectious potential (Chagas et al, 2021;Scorza et al, 2021).…”

Possibility of Leishmania Transmission via Lutzomyia spp. Sand Flies Within the USA and Implications for Human and Canine Autochthonous Infection

“…More recently, Scorza et al (2021) demonstrated that this population of hunting dogs has an abundant dermal parasite burden and that subclinical animals transmitted Leishmania parasites during xenodiagnoses to Lu. longipalpis [ 46 ••]. Lu.…”

“…Lu. longipalpis ingested parasites from the skin of dogs with mild to moderate clinical disease [ 46 ••], which suggests that healthy-appearing, vertically infected dogs can transmit parasites to sand flies and propagate emergence of L. infantum in locations where Lu. longipalpis or other competent vector species were present [ 46 ••].…”